imm Associationsi from m tile Fossil Record URBAN STONE DECAY .•---sc- Plant-Insect • t-i-.i*'^ & Associations ^-''•:^ FROM THE Fossil Record v>i:::=^ r The coarsest characterization of life on Earth is probably one of teeming diversity. As terrestrial organisms ourselves, we are impressed by the enormous variety of -.^ life on land, and in particular, by the countless taxa of insects and vascular plants that constitute much of the écologie underpinning for terrestrial ecosystems. Any understanding of this diversity requires documentation of the associations among these two most pervasive groups of organisms. Historically, vascular plants and insects have provided the requisite numbers of species to support Ü\is ever-widening web of écologie interdependence. We know from the earhest fossils that only a few species of insects co-existed with primitive plants during the Early Devonian, principally as detritivores with monotonous diets of dead tissues, but also as a few nonspecialized herbivores. However, 400 miUion years later, after evolutionary radiations of land plants had produced complex ecosys- tems, approximately 280,000 species of vascular plants and several million to a few tens of millions of insects came to dominate the terrestrial world. Integral to this escalation of plant and insect numbers are the associations among these organisms, which • together with interacting fungi • represent a significant multiple of the individual • A diversities of the principal actors. 'i^^'îïy^- Consider a milkweed plant. Within a single photosynthesizing individual, a dozen species of herbivorous insect consumers can co-exist • each with a particular mouth- part structure for targeting a specific tissue type within leaves, stems, roots, and repro- ductive structures. These insects, in turn, are devoured internally by parasitoids or V- externally by parasites, each of which is attacked by hyperparasitoids, and all of which are preyed upon in complex ways by mobile and stationary insect predators. '^. How did such intricate trophic networks originate? Is there documentation in the fos- sil record, either from the organisms themselves or from their interactions, that can illu- minate the general pattern of this increasing complexity? Can we say anything about ;/?.;-. i; species-generating processes that may be revealed by the fossil record of plant-insect associations? 'i by Conrad C. Labandeira Geotinaes • September 1998 MACROEVOLUTIONARY STUDY OF PLANT-INSECT ASSOCIATIONS The answer to all of these questions is a qualified "yes," but so far, only prelimi- nary results have been reached. Consider a milkweed Examination and interpretation of the fossil record of plant-insect interactions plant. Within a is a new field within paleobiology, histor- ically ignored by both paleoentomolo- single photosynthesizing gists and paleobotanists and rarely dis- cussed by today's biologists studying the individual, a dozen species myriad associations between modern plants and insects. Virtually all of the of herbivorous insect existing paleobiological literature on this topic consists of descriptions of interest- consumers can co-exist. ing interactions with fossil plants, and several recent hypotheses of how insects and plants associate at macroevolution- respective host-plants, in lieu of direct ary time scales have not been addressed. fossil evidence. In this alternative Recently, phylogenetic data have been approach, molecular-based phylogenies marshaled to understand the macroevo- for plant hosts and their insect herbi- lutionary histories of selected lineages vores are established in order to deter- of extant insect herbivores and their mine if diversification occurred in paral- génies (Figure I). Rarely, however, are lel, as evidenced by the congruence of such studies explicitly calibrated by plant host and insect herbivore phylo- specimens from the fossil record; rather, they rely on a molecular clock for esti- mates of the origins of particular plant and insect taxa. Such an approach is not beetle herbivore associations hiost plant phylogeny phylogeny available for extinct lineages of asso- Hoplasoma -* *- Clerodendrum ciated plants and insects. A more direct approach is to docu- Slachyslvora -*- ment highly invariant, repeatable types of insect damage on well-preserved fos- P. quadrjmacuiata sil floras to establish distinctive patterns -^f~ S. galeficulala P. decórala •< :> of tissue use by host herbivores. -*- S. integriilolia Temporal trends gleaned from this approach may reveal evolutionary radia- • • gf tions of certain herbivore clades onto plant taxa, or more particularly, the P. costpennis -^- trajectory of host specificity through II' time. For host specificity by insects, a P. sp. nou. -^- -^ S. mosna continuum is well known. ÍÍ sororia -*- -*- S. drummondi P. physostegiae -*- S laterillora -*^hysostegla Figure 1. A comparison of the phylogenies of the Phyilobrotica clade of leaf Ijeeties (Chrysomelidae) and their host-plant clade of Scutellaria and related mint taxa {Lamiaceae), taken and modified fi'om Farrell and Mitter (1990). Note close correspondence between beetles and their host plants, with the notable exception of host switching of P. physostegae on Physoste^a. September 1998 • Geotimes soft Representing one extreme is one-to- one fidelity between an insect herbivore and its plant liost; the other extreme is rampant host-switching or collective extinction (Figure 2). A particularly intriguing method that has never been attempted in the fossil record is to track a well-established plant lineage of a few taxa through macroevo- lutionary time and monitor the spectrum of insect herbivores. Documentation of herbivore types through time can estab- lish if some insect and plant lineages are ancient associations or whether older associations are being swamped con- stantly by more recently evolved insect herbivores. If the plant host is highly con- fined taxonomically • say, a group of related species, a genus, or a nondiverse family • the fossil record can be used to examine approximately what modem biologists term a "component commu- nity." A component community constitutes all the animal associates of a particular plant-host species (Figure 3). Tracking insect herbivory within a component community, based on recognition of dam- age types, can provide data on the entries, exits, and protracted associa- tions of insect herbivore species in macroevolutionary time. Such paleobio- logical data could answer questions of high theoretical importance • such as whether co-evolved and longer-term associations occur between plants and insects, if primitive insects occur on primitive plants, or whether host-switch- ing is associated with raEyor paleoenvi- ronmental changes or with the physical features of plant hosts. :l /•:• Figure 2. Two examples of associations iaetween leaf-mining insects and their host piants, gleaned from the fossil record of plant damage. The upper part of the figure (a) depicts an ancient •W association between an insect herbivore, the leaf-mining moth Ectoedemia, and its host plant, an undescribed form closely related to the sycamore Platsnus, from the mid-Cretaceous Dakota Formation of Kansas. The inset in the center (b) is an enlargement of this leaf mine, showing ini- tial serpentine phase and subsequent blotch phase lodged between two primary veins. The leaf on the right (c) contains near-identical Ectoedemia damage on modem Platanus from Virginia. The lower pair show either temporal host-switching or extinction of both plant host and a species of the leaf-mining moth Paraclemensia or a closely related genus. The lower-left leaf (d) exhibits Parac/emens/3-like damage on its Middle Eocene host plant Macginitiea, an extinct genus of the sycamore family from the Green River Formation of Utah. The lower-right leaf (e) features near- idenfcal Paraclemensia damage on modem Acer irom Vermont, a member of the maple family that is phylogenetlcally distant from sycamores. Scale bars: solid = 1.0 cm; striped = 0.1 cm. Geotimes • September INCREASED INTENSITY OF INSECT HERBIVORY A second general area of paleobiological investigation involves the evaluation of insect herbivory intensity through time. Quantifying the percentage of fossil leaf area removed by insects in fossil floras has been attempted only recently, although such studies are now routine in extant tropical to warm-temperate floras. For us to understand temporal trends in insect herbivory intensity • particularly within ecologically constrained plant- conununity types • requires a test of the "Red Queen Hypothesis." This hypothesis predicts that because insects continually adapt to circumvent defenses of their plant hosts while, conversely, plant hosts develop mechanisms to ward off insect herbivory, a progressive "arms race" takes place. In other words, both herbi- vore and host are "running faster and faster just to stay in place," similar to the phght of Alice and the Red Queen in Figure 3. A component community of insect herbivores on a iiypothetical vascuiar plant. Included Through the Looking Glass. Applying are piercer-and-suchers at top (a, b) and center right (c), borers at center (d^), serpentine and this rule to the fossil record of insect her- blotch leaf miners at lower right (h), leaf and twig gailers at left <i-k), and extemai feeders at lower- left (I) and bottom (m). I\/lodified fj-om Johnson and Lyon (1991). Reprinted with permission trom bivory, the question becomes: Is there Cornel! University Press. © 1991. evidence for escalation